Dicrocoelium Dendriticum Found in a Bronze Age Cemetery in Western

Parasitology International 64 (2015) 251–255

Contents lists available at ScienceDirect

Parasitology International

journal homepage: www.elsevier.com/locate/parint

Dicrocoelium dendriticum found in a Bronze Age cemetery in western Iran in the pre-Persepolis period: The oldest Asian palaeoﬁnding in the present human infection hottest spot region

Gholamreza Mowlavi a,⁎, Kobra Mokhtarian b, Mahsa Sadat Makki a,IrajMobedia, Mohammad Masoumian c, Reza Naseri d, Ghasem Hoseini e,ParisaNekoueic, Santiago Mas-Coma f,⁎⁎ a Department of Medical Parasitology and Mycology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran b Medical Plants Research Center, Shahrekord University of Medical Sciences, Shahrekord, Iran c Department of Archeology, Faculty of Literature and Humanities, Tehran University, Tehran, Iran d Department of Archeology, Faculty of Art and Architecture, Zabol University, Zabol, Iran e Department of Medical Parasitology and Mycology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran f Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot, Valencia, Spain article info abstract

Article history: Dicrocoeliasis of animals and humans is caused by trematode species of the genus Dicrocoelium,mainly Received 13 January 2015 Dicrocoelium dendriticum in ruminants of the Holarctic region. D. dendriticum may be considered an old parasite, Received in revised form 12 February 2015 probably related to the appearance and diversification of Eurasian ovicaprines, occurred 14.7–14.5 million years Accepted 25 February 2015 ago. The oldest palaeoparasitological findings of Dicrocoelium in domestic animals and humans date from more Available online 6 March 2015 than 5000 years BC in Europe. Eggs of D. dendriticum have been found in a burial of a Bronze Age cemetery – fi Keywords: (2600 2200 BC) close to Yasuj city, southwestern Iran. This is the oldest nding of D. dendriticum in the Near Dicrocoelium dendriticum East, where present human infection reports are more numerous than in other world regions where human Eggs dicrocoeliasis is rare and sporadic. This palaeofinding in the Zagros mountainous chain area is of interest by its Burial remains location close to Persepolis, suggesting a narrow relationship between humans and herbivorous animals in Bronze Age cemetery these highlands. Domestic ruminant populations of these highlands were following a repeated contact with 2600–2200 BC those of the western flat lowlands of the Fertile Crescent thanks to annual altitudinal transhumance migrations Iran of the nomadic pastoral tribes with their herds living throughout Zagros Mountains in the several millennium period BC. It is concluded that D. dendriticum spread together with sheep and goats westward throughout Europe from the Fertile Crescent during the 8000–6000 year BC period and somewhat later southward into Africa, both spreads facilitated by the low specificity of that trematode species regarding the snail and ant intermediate hosts. © 2015 Elsevier Ireland Ltd. All rights reserved.

1. Introduction 2–2.5 mm, and which is commonly known as the lancet fluke, the lance- olate fluke, the little liver fluke or the small liver fluke. It shows a scarce Dicrocoeliasis is a trematodiasis caused by digenean species of the definitive host specificity, although with pronounced preference for ru- genus Dicrocoelium (Trematoda: Dicrocoeliidae), mainly Dicrocoelium minants which may be considered the true original hosts, among which dendriticum (=Dicrocoelium lanceolatum) throughout and Dicrocoelium mainly mid-sized ruminants as sheep and goats and secondarily large hospes in Africa southward from the Sahara. The adult stage is a parasite ruminants as cattle. Their transmission involves a three host life cycle, of the bile ducts and gall bladder, of a relatively small size of about 8–14/ with embryonated eggs of 35–45/22–30 μm expelled with the mammal feces, to follow a completely terrestrial life cycle. Many terrestrial snail species act as first intermediate hosts, with differences depending on ⁎ Correspondence to: G. Mowlavi, Department of Medical Parasitology & Mycology, the geographical area. Several ant species, mainly belonging to the School of Public Health, Tehran University of Medical Sciences, Iran, P.O. Box 6446, Tehran 14155, Islamic Republic of Iran. Tel./fax: +98 2188951392. genus Formica, act as second intermediate hosts inside which the infec- ⁎⁎ Correspondence to: S. Mas-Coma, Departamento de Parasitologia, Facultad de tive metacercariae develop. The ruminant hosts become infected by Farmacia, Universidad de Valencia, WHO Collaborating Centre on Fascioliasis and Its ingesting these ants when grazing [1]. Snail Vectors, FAO-United Nations Reference Centre for Parasitology, Av. Vicent Andres Infection by D. dendriticum is an important parasitic disease in ani- Estelles s/n, 46100 Burjassot, Valencia, Spain. Tel.: +34 96 354 42 98; fax: +34 96 354 mals from an economic and health viewpoint [2]. In humans, clinical 47 69. fi E-mail addresses: [email protected] (G. Mowlavi), [email protected] symptoms of true dicrocoeliosis are neither uniform nor speci c. As (S. Mas-Coma). with other liver fluke infections, the pathology depends on the number

http://dx.doi.org/10.1016/j.parint.2015.02.007 1383-5769/© 2015 Elsevier Ireland Ltd. All rights reserved. 252 G. Mowlavi et al. / Parasitology International 64 (2015) 251–255 of flukes present and the duration of the infection. Because of the small the interesting relationships of the mountainous area in question with size of the fluke and its smooth and spineless surface, mechanical and the western flat lowlands of the Fertile Crescent by means of nomadic toxic damages are much less than in fascioliasis and opisthorchiasis tribes practicing altitudinal transhumance with their herds. [1]. Moreover, the main route of migration of D. dendriticum to reach the liver is via the bile ducts, instead of via the abdominal cavity route 2. Materials and methods as in Fasciola hepatica [3]. Highly pathogenic infections in humans have been however described, as rare neurological symptoms and sub- Specimens including soil samples obtained from three burials and sequent meningeal syndrome [3,4] and recently also involvement in an one burial jar were collected during a rescue excavation in a Bronze “ ” allergic pharyngitis syndrome known as Halzoun [5]. Humans acquire Age cemetery (2600–2200 BC) located in the neighborhood of the city the infection accidentally, by swallowing an infected ant together with of Yasuj, Kohkilooye and Boyer-Ahmad province, in southwestern the food, such as vegetables, fruits, etc., while staying in an endemic Iran, in the late winter 2012. The archeological remains are located at area. 70 km northwestward of the aforementioned city, at the coordinates This parasite species has a more or less cosmopolitan distribution in of 31°9′13″ N and 51°6′14″ E(Fig. 1). Excavation procedures were herbivorous mammals, mainly in ruminants of the Holarctic region. The undertaken in a way to prevent burial materials to be contaminated parasite is believed to have been introduced into the New World with with external soil. the extensive importations of dairy cattle from European countries. Archeological dating was comparatively proved, based on potteries Human infections have been recorded in D. dendriticum enzootic and bronze items found in the graves. For the retrieving of helminth areas. Although the majority of these infections are of rare and sporadic eggs, the rehydration technique in 0.5% trisodium phosphate was occurrence, they are undoubtedly underestimated. Most infections are used, according to the method successfully practiced so far [17].Recov- only spurious, the appearance of eggs in stools being due to the inges- ered eggs were photographed, measured and identified morphological- tion of infected livers of sheep, goat and cattle, eggs being detected in ly, according to available references. feces for only a few days. The reason for the availability of infected animal livers on the market is that not all infected livers show signs of the infection. Genuine human infection can be verified through parasite 3. Results finding in surgical operations, evidence of permanent egg shedding through time, egg recovering in duodenal aspirates, or the existence of A total of 1100 slides from rehydrated soil samples were thoroughly related symptomatology. Human infection has been reported from investigated under the light microscope. During this careful microscopic Asia, northern Africa, Europe, North America and South America [1]. investigation, 750 slides were also thoroughly examined for the eventu- D. dendriticum may be considered an old parasite, probably related al detection of helminth eggs. fi to the appearance of Eurasian ovicaprines. The diversification of Two eggs showing typical trematode features could be identi ed in Caprinae occurred 14.7–14.5 million years ago (mya) and the diver- grave N2 (Fig. 2). When microscopically measured, these eggs proved gence of Ovis and Capra 11.3 mya, the later species diversification within to be brown, thick-shelled and with an inconspicuous operculum, of a μ these two genera having been dated around 5.1 to 6.8 mya [6].Wildher- size of 38.9/23.0 m of length/maximum width, in an excellent conser- bivore domestication began around 10,000 years ago at the dawn of the vation condition and even allowing for the distinction of miracidium Neolithic in the region known as the Fertile Crescent, a formerly fertile, remains inside. now partly desert, area in the Near and Middle East which was an agri- cultural region extending from the Levant (lands bordering the Eastern 4. Discussion shores of the Mediterranean and Aegean seas) eastward including modern-day Israel, Jordan, Lebanon and western Syria, into southeast The characteristics and size of the trematode eggs found fully agree Turkey and, along the Tigris and Euphrates rivers, into Iraq and the with those of the eggs of the species D. dendriticum, which are known western flanks of Iran [7–10]. The Neolithic period was an era of to have a length/width range of 35–45/22–30 μm [18]. The finding in major changes in human life. Goats, in the form of their wild progenitor the northern hemisphere allows for the ruling out of the other species the bezoar Capra aegagrus, also called Persian wild goat [11],werethe also infecting humans, D. hospes, with similar eggs but restricted to first wild herbivores to be domesticated. Sheep and goat domestication the African continent [1]. played an important role in the phenomenon of Neolithization occur- In Asia, there are no palaeoparasitological findings of Dicrocoelium ring in the late prehistory of the Near and Middle East between 9000 [19,20], except the only very recent one in an ancient salt mine in and 5000 BC. Data from the numerous neolithic human settlements Chehrabad, northwestern Iran, around 2500–1500 years BP [21]. Our found throughout this region strongly point to it as a major domestica- finding becomes thus the oldest one of D. dendriticum in Asia and the tion center for livestock species, mainly goats and sheep [12]. second palaeoparasitological finding in Iran. Ovicaprine domestication gave rise to the transition from a nomadic This report being the oldest palaeoparasitological finding of D. to a sedentary way of life [13], human life becoming close to that of dendriticum in Iran is somehow surprising, as indeed the Near East these mid-sized and readily mobile ruminants and thus also to their (Fig. 1) is the only region of the world in which present human infection parasites. reports are clearly more numerous than in other regions where human The oldest record of Dicrocoelium was made in mammal coprolites dicrocoeliasis only appears to be rare and sporadic. dated from the Middle Pleistocene in France, 550,000 years BP [14]. In Turkey, in the last century a report referred seven mature D. Palaeoparasitological findings of Dicrocoelium do afterwards only ap- dendriticum in a 26-year-old woman after a gall bladder operation [22] pear in sites of 5259 years BC in Germany and in 3917–1750 years BC and this trematode was found in 0.96% among 6311 patients [23]. in France, Germany, Switzerland, in 3365–2600 years BC in Sudan and Other reports in Turkey were published in the first decade of the present Iron age in South Africa, and later, already in different centuries AD in century [24–32], of which several reported severe pathogenicity [28, these European countries plus Austria and England [15],andalsoin 31]. Saudi Arabia stands out by the high number of patients diagnosed the 17th century in Canada [16]. expelling eggs in their feces [33–37]. In Iran, reports refer to human in- The present study deals with the palaeoparasitological finding of D. fection in different parts of the country and since long time [38–40].This dendriticum in an archeological remain in the neighborhood of the city human dicrocoeliasis hot spot area may be even considered to be spread of Yasuj, in southwestern mountainous Iran. Besides the description of more eastward, as suggested by the finding of D. dendriticum adults in the egg materials found, focus is made on the closeness with the ancient the livers (up to 4 flukes/liver) of 37 of the 13,287 corpses autopsied city of Persepolis, the ceremonial capital of the Achaemenid Empire, and from 1968 to 1986 in Uzbekistan, in which infection was reported to G. Mowlavi et al. / Parasitology International 64 (2015) 251–255 253

Fig. 1. Map of the Near East showing the location of the Bronze Age cemetery in the neighborhood of the city of Yasuj, in Iran, where Dicrocoelium dendriticum eggs were found in a grave, geographical distribution covered by the ancient Fertile Crescent around the rivers Euphrates and Tigris, and present countries included in the Dicrocoelium dendriticum human infection hottest region of nowadays. Note geographical closeness of aforementioned cemetery to Persepolis and Ahwaz.

be the cause of death in no case, nor was the infection ever diagnosed during life [41]. ThepresenceofD. dendriticum since thousands of years, as indicated by the palaeoparasitological finding of our report, may be interpreted as a parasite being well established and widely distributed in that region. Consequently, additional palaeoparasitological findings of D. dendriticum in future archeological explorations, whether in domestic livestock or in humans, might be expected, even older than the one described in this study. This hypothesis is also supported by the widespread dicrocoeliasis in Iranian ruminants [42,43], as well as by the low specificity of D. dendriticum at the level of terrestrial snail host and ants second intermediate hosts (different widespread species of Formica and related genera) [44–46]. Indeed, the principal human source of dicrocoeliasis becomes infected sheep with extremely high worm loads (up to 108,000 worms), and a very high level of incidence of infection (often 100%). The consequence is a high rate of pasture infestation resulting from fecal contamination, which is in turn potentiated by large-scale, inten- sive breeding of these animals. The great quantity of eggs laid by a single Fig. 2. Egg of Dicrocoelium dendriticum found in a grave of a Bronze Age cemetery, dated fluke during its several-year life-span is multiplied many times by the 2600–2200 years BC, in the neighborhood of the city of Yasuj, in Iran. larval stage multiplication at snail host level. This is responsible for the 254 G. Mowlavi et al. / Parasitology International 64 (2015) 251–255

Fig. 3. Stone wall illustrations of life scenes including domesticated mid-sized and large sized ruminants in the present ruins of Persepolis, the ancient ceremonial capital of the Achaemenid Empire, dated from around 515 BC.

heavy infestation of the pasture environment, especially under favor- Archeozoological analyses showed that sheep and goats had been able conditions [1]. imported into the Euphrates mid-valley already around 8200– Additionally, this D. dendriticum egg finding in the neighborhood of 8000 years BC [51]. Evidence by ancient DNA analysis of 8000 BC near Yasuj, in the Zagros mountainous chain area, is of special interest by its eastern farmers has supported an early neolithic pioneer maritime col- geographical location, which appears to be (i) southward close to Persep- onization of mainland Europe through Cyprus and the Aegean islands olis and (ii) westward close to the original Fertile Crescent flat lowlands. [52]. Therefore, it may be concluded that D. dendriticum spread together Persepolis is located at 1630 m high altitude and only around with sheep and goats westward throughout Europe from the Fertile 150 km southeast of Yasuj. The earliest remains of this ancient city Crescent during the 8000–6000 year BC period and somewhat later date from around 515 BC, that is, around 2000 years later than the cem- southward into Africa, both spreads facilitated by the low specificity of etery discovered at 1500 m high altitude close to Yasuj, a city which is that trematode species regarding the snail and ant intermediate hosts. nowadays located at 1800 m altitude (Fig. 1). However, Persepolis This agrees with the palaeoparasitological review on Dicrocoelium data archeological ruins, located at 1630 m high altitude, offer interesting from domestic livestock and humans throughout Europe and Africa reliefs, illustrating animal domestication throughout the highlands of [15]. Hence, it may be concluded that the oldest record of Dicrocoelium the Zagros mountainous chain area. Thus, sheep, goats and zebu cattle in mammal coprolites dated from the Middle Pleistocene in France, (Fig. 3), the main definitive hosts of D. dendriticum, but also other poten- 550,000 years BP [14],wasindeednotinvolvingD. dendriticum but tial hosts such as donkeys, horses, camels and dromedaries [1],appear other dicrocoeliid species. repeatedly in the scenes illustrated on the stone walls of the ancient Persepolis buildings. This speaks about a close relationship between humans and these herbivorous animals also in the highlands in ques- Acknowledgments tion. The geographical proximity of the Yasuj palaeofinding and Persep- olis highlights the common feature of an altitude area, which is of great Thanks are given to the Iranian Center for Archeological Research importance for the life cycle and snail vectors of trematodes [12]. (ICAR) for facilities provided during the excavation project and trusting Additionally, all indicates that the domestic ruminant populations of us with the study of burial soil. these highlands were following a more or less continuous contact with Spanish collaboration funded by the project No. RD12/0018/0013, — those of the western flat lowlands of the Fertile Crescent thanks to an- Red de Investigación Cooperativa en Enfermedades Tropicales RICET, – — nual altitudinal transhumance migrations (from the lowlands in cold of the National Program I + D + I 2008 2011, ISCIII Subdirección months to the highlands in hot months) of nomadic pastoral human General de Redes y Centros de Investigación Cooperativa, Ministry of groups with their herds coexisting with sedentary people living in per- Health and Consumption, Madrid, Spain, and Project PROMETEO/2012/ manent Neolithic settlements throughout the Zagros mountainous 042, of the program of Ayudas para Grupos de Investigación de chain area in the several millennium period BC [47–50].Severalof Excelencia, Generalitat Valenciana, Valencia, Spain. these nomadic tribes (Boyerahmadi, Bahmaei, Qashqai and Bakhtiari) are still practicing altitudinal transhumance in the Iranian province of References Yasuj city (Kohkilooye and Boyer Ahmad) and neighboring provinces (Khuzestan, Chahar Mahaal and Bakhtiari, Isfahan, and Fars) nowadays. [1] Mas-Coma S, Bargues MD. Human liver flukes: a review. Res Rev Parasitol 1997;57: The presence of D. dendriticum in the western lowland area of Ahwaz 145–218. [2] Wolff K, Hauser B, Wild P. Dicrocoeliose des Schafes: Untersuchungen zur (Khuzestan province) [43] is an additional support to the aforemen- Pathogenese und zur Regeneration des Leber nach Therapie. Berl Munch Tierarztl tioned considerations (Fig. 1). Wochenschr 1984;97:378–87. G. Mowlavi et al. / Parasitology International 64 (2015) 251–255 255

[3] Mas-Coma S, Agramunt VH, Valero MA. Neurological and ocular fascioliasis in [27] Degerli S, Ozçelık S, Celiksöz A. The distribution of intestinal parasites in patients humans. Adv Parasitol 2014;84:27–149. presenting at the parasitology laboratory of the Cumhuriyet University. Acta [4] Siguier F, Feld R, Piette M, Welti JJ, Lumbroso P. Tribulations neurologiques d'un Parasitol Turc 2005;29:116–9. jeune berger atteint de distomatose cérébrale à Dicrocoelium lanceolatum.Bull [28] Karadag B, Bilici A, Doventas A, Kantarci F, Selcuk D, Dincer N, et al. An unusual case Mem Soc Med Hop Paris 1952;68:353–9. of biliary obstruction caused by Dicrocoelium dentriticum.ScandJInfectDis2005;37: [5] Khalil G, Haddad C, Otrock ZK, Jaber F, Farra A. Halzoun, an allergic pharyngitis 385–8. syndrome in Lebanon: the trematode Dicrocoelium dendriticum as an additional [29] Culha G. The distribution of patients with intestinal parasites presenting at the par- cause. Acta Trop 2013;125:115–8. asitology laboratory of the Mustafa Kemal University Medical Faculty. Acta Parasitol [6] Hernandez Fernandez M, Vrba ES. A complete estimate of the phylogenetic relation- Turc 2006;30:302–4. ships in Ruminantia: a dated species-level supertree of the extant ruminants. Biol [30] Ataş AD, Alim A, Ataş M. Distribution of intestinal parasites in patients presenting at Rev 2005;80:269–302. the environmental-food and medicine analysis laboratory of Sivas municipality [7] Bruford MW, Bradley DG, Luikart G. DNA markers reveal the complexity of livestock during the years 1993–2006. Acta Parasitol Turc 2008;32:59–64. domestication. Nat Rev Genet 2003;4:900–10. [31] Soyer T, Turkmen F, Tatar N, Bozdogan O, Kul O, Yagmurlu A, et al. Rare gallbladder [8] Peters J, Helmer D, Von Den Driesch A, Segui MS. Early animal husbandry in the parasitosis mimicking cholelithiasis: Dicrocoelium dendriticum. Eur J Pediatr Surg Northern Levant. Paléorient 1999;25:27–47. 2008;18:280–1. [9] Mac Hugh DE, Bradley DG. Livestock genetic origins: goats buck the trend. Proc Natl [32] Cengiz ZT, Yilmaz H, Dulger AC, Cicek M. Human infection with Dicrocoelium Acad Sci U S A 2001;98:5382–4. dendriticum in Turkey. Ann Saudi Med 2010;30:159–61. [10] Zeder M. A view from the Zagros: new perspectives on livestock domestication in [33] Bolbol AHS. Some unusual parasitic infestation reported at King Abd Al-Aziz the Fertile Crescent. In: Vigne JD, Peters J, Helmer D, editors. First steps of animal do- Teaching Hospital, Riyadh, Saudi Arabia. J Egypt Soc Parasitol 1985;15:23–7. mestication. New archaeozoological approaches. Oxford: Oxbow Books; 2005. [34] Mohamed ARE, Mummery V. Human dicrocoeliasis. Report on 208 cases from Saudi p. 125–46. Arabia. Trop Geogr Med 1990;42:1–7. [11] Potts DT. Ibex, Persian. Encyclopaedia Iranica; 2004;12(6):613–5. [35] Khan ZA, Al Jama AAA, Namnyak SS, Regalado M. Dicrocoelium dendriticum in Saudi [12] Mas-Coma S, Valero MA, Bargues MD. Fasciola, lymnaeids and human fascioliasis, Arabia. Saudi Med J 1988;9:391–3. with a global overview on disease transmission, epidemiology, evolutionary genet- [36] Omar MS, Abu-Zeid HAH, Mahfouz AAR. Intestinal parasitic infections in ics, molecular epidemiology and control. Adv Parasitol 2009;69:41–146. schoolchildren of Abha (Asir), Saudi Arabia. Acta Trop 1991;48:195–202. [13] Vigne JD. Zooarchaeological aspects of the Neolithic diet transition in the Near East [37] Helmy MM, Al-Mathal EM. Human infection with Dicrocoelium dendriticum in and Europe, and their putative relationships with the Neolithic demographic transi- Riyadh district (Saudi Arabia). J Egypt Soc Parasitol 2003;33:139–44. tion. The Neolithic demographic transition and its consequences. The Netherlands: [38] Farid H. Human infection with Fasciola hepatica and Dicrocoelium dendriticum in Springer Science and Business Media B.V; 2008. p. 179–205. Isfahan area, Central Iran. J Parasitol 1971;57:160. [14] Jouy-Avantin F, Combes C, de Lumley H, Miskovsky JC, Moné H. Helminth eggs in an- [39] Sohrabi A. Human dicrocoeliasis: 2 case reports from Iran. Iran J Publ Health 1982/ imal coprolites from a middle Pleistocene site in Europe. J Parasitol 1999;85:376–9. 1983;11:55–6. [15] Le Bailly M, Bouchet F. Ancient dicrocoeliosis: occurrence, distribution and migra- [40] Ashrafi K. Human dicrocoeliasis in northern Iran: two case reports from Gilan tion. Acta Trop 2010;115:175–80. province. Ann Trop Med Parasitol 2010;104:351–3. [16] Horne PD, Tuck JA. Archaeoparasitology at a 17th century colonial site in Newfound- [41] Azizova OM, Sagieva AT, Israilova S, Sadykov VM, Shirinova NS, Mukhitdinov SM, land. J Parasitol 1996;82:512–5. et al. Dicrocoelium lanceolatum infection in man (on autopsy data). Meditsinsk [17] Reinhard KJ, Confalonieri UE, Herrmann B, Ferreira LF, de Araujo AJG. Recovery of Parazitol Parazit Bol 1988;2:26–8 [in Russian]. parasite remains from coprolites and latrines: aspects of paleoparasitological [42] Ansari-Lari M, Moazzeni M. A retrospective survey of liver fluke disease in livestock technique. Homo 1986;37:217–39. based on abattoir data in Shiraz, south of Iran. Prev Vet Med 2006;73:93–6. [18] Mas-Coma S, Bargues MD, Marty AM, Neafie RC. Hepatic trematodiases. In: Meyers [43] Ahmadi NA, Meshkehkar M. Prevalence and long term trend of liver fluke infections WM, Neafie RC, Marty AM, Wear DJ, editors. Pathology of infectious diseases, vol. in sheep, goats and cattle slaughtered in Khuzestan, southwestern Iran. J Paramed 1 helminthiases. Washington DC: Armed Forces Institute of Pathology and Sci 2010;1:26–31. American Registry of Pathology; 2000. p. 69–92. [44] Rosicky B, Groschaft J. Dicrocoeliosis. In: Hillyer GV, Hopla CE, editors. Handbook se- [19] Araujo A, Ferreira LF. Parasite findings in archeological remains: a paleogeographic ries in zoonoses. Section C. Parasitic zoonoses, vol. III. Boca Raton-Florida: CRC Press; view. The findings in Asia. In: Ferreira LF, Reinhard KJ, Araujo A, editors. Foundations 1982. p. 33–52. of paleoparasitology. Rio de Janeiro: Editora Fiocruz; 2014. p. 389–95. [45] Manga-Gonzalez MY, Gonzalez-Lanza C. Field and experimental studies on [20] Fornaciari G, Gaeta R. Paleoparasitology of helminths. In: Bruschi F, editor. Helminth Dicrocoelium dendriticum and dicrocoeliasis in Northern Spain. J Helminthol 2005; infections and their impact on global public health. Wien: Springer-Verlag; 2014. 79:291–302. p. 29–47 [Chapter 2]. [46] Manga-González MY, González-Lanza C, Cabanas E, Campo R. Contributions to and [21] Nezamabadi M, Aali A, Stöllner T, Mashkour M, Le Bailly M. Paleoparasitological review of dicrocoeliosis, with special reference to the intermediate hosts of analysis of samples from the Chehrabad salt mine (Northwestern Iran). Int J Dicrocoelium dendriticum. Parasitology 2001;123:S91–S114. Paleopathol 2013;3:229–33. [47] Ullens de Schooten MT. Lords of the mountains: Southern Persia and the Kashkai tribe. [22] Coskuner S, Tamkan A, Merter T, Ang Ö. A case report of dicrocoeliasis in a woman. London: Chatto and Windus Ltd., The Travel Book Club; 1956 p. 53–4p.114–8. Turkiye Parazitol Derg 1979;2:31–7 [in Turkish]. [48] Ramazani R. The Northern Tier: Afghanistan, Iran and Turkey. New Jersey: D. Van [23] Kiliçturgay K, Gokirmak F, Tore O, Soysal G. The distribution of enteric parasites Nostrand Company; 1966 85. in the Bursa region over 5 years. Turkiye Parazitol Derg 1982;5:15–21 [in [49] Mashkour M. Tracing ancient ‘nomads’: (1) isotopic research on the origins of verti- Turkish]. cal ‘transhumance’ (2) in the Zagros region. Nomadic People 2003;7(2):36–47. [24] Öner YA, Sahip N, Uysal H, Buget E. Parasitological findings in 15,714 stool samples [50] Devolder M. La transhumance des nomades iraniens, une richesse culturelle between the years 1997 and 2001 at the Parasitology Department of the Ïstanbul mondiale. La Revue de Teheran 2006;12:1–2. Medical Faculty. Acta Parasitol Turc 2002;26:303–4. [51] Vigne JD. Les débuts néolithiques de l'élevage des bovidés et de l'éxploitation laitière [25] Demirel MM, Ïnceboz T, Tosun S. Investigation of intestinal parasites in patients dans l'Ancien Monde. In: Poulain JP, editor. L'homme, le mangeur et l'animal. Qui presenting at the Manisa Morris Şinasi Children's Hospital in the region of central nourrit l'autre?Paris: Les Cahiers de l'Ocha; 2007. p. 45–57. Manisa. Acta Parasitol Turc 2003;27:262–5. [52] Fernandez E, Perez-Perez A, Gamba C, Prats E, Cuesta P, Anfruns J, et al. Ancient DNA [26] Alver O, Ozakin C, Yilmaz E, Akçağlar S, Töre O. Evaluation of the distribution of analysis of 8000 BC near eastern farmers supports an early neolithic pioneer mari- intestinal parasites in the Uludağ University Medical Faculty during a period of time colonization of mainland Europe through Cyprus and the Aegean islands. eight years. Acta Parasitol Turc 2005;29:193–9. PLoS Genet 2014;10(6):e1004401 [16 pp.].